The underestimated role of roots in defense against leaf attackers

Erb, Matthias; Lenk, Claudia; Degenhardt, Jörg; Turlings, Ted C. J.

doi:10.1016/j.tplants.2009.08.006

Cited by 167 publications

(171 citation statements)

References 93 publications

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“…Several other compounds, including tropane alkaloids in Solanaceae species (Ziegler and Facchini, 2008) and pyrrolizidine alkaloids in Asteraceae (Hartmann and Ober, 2000), have been shown to follow a similar pattern of synthesis in roots followed by translocation to leaves. These examples have led to the appreciation that roots play important roles in the aboveground defensive mechanisms (Erb et al, 2009). Only LC and not SC aliphatic GLS seem to be primarily made in roots and distributed to other parts of the plant.…”

Section: Integration Of Biosynthesis and Transport In Plant Defenses?mentioning

confidence: 99%

Integration of Biosynthesis and Long-Distance Transport Establish Organ-Specific Glucosinolate Profiles in VegetativeArabidopsis

et al. 2013

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Although it is essential for plant survival to synthesize and transport defense compounds, little is known about the coordination of these processes. Here, we investigate the above-and belowground source-sink relationship of the defense compounds glucosinolates in vegetative Arabidopsis thaliana. In vivo feeding experiments demonstrate that the glucosinolate transporters1 and 2 (GTR1 and GTR2), which are essential for accumulation of glucosinolates in seeds, are likely to also be involved in bidirectional distribution of glucosinolates between the roots and rosettes, indicating phloem and xylem as their transport pathways. Grafting of wild-type, biosynthetic, and transport mutants show that both the rosette and roots are able to synthesize aliphatic and indole glucosinolates. While rosettes constitute the major source and storage site for short-chained aliphatic glucosinolates, long-chained aliphatic glucosinolates are synthesized both in roots and rosettes with roots as the major storage site. Our grafting experiments thus indicate that in vegetative Arabidopsis, GTR1 and GTR2 are involved in bidirectional longdistance transport of aliphatic but not indole glucosinolates. Our data further suggest that the distinct rosette and root glucosinolate profiles in Arabidopsis are shaped by long-distance transport and spatially separated biosynthesis, suggesting that integration of these processes is critical for plant fitness in complex natural environments.

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Section: Integration Of Biosynthesis and Transport In Plant Defenses?mentioning

confidence: 99%

Integration of Biosynthesis and Long-Distance Transport Establish Organ-Specific Glucosinolate Profiles in VegetativeArabidopsis

et al. 2013

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“…Therefore it is possible that roots may direct the signaling that causes a rapid shuttling of resources to roots following herbivory and subsequent return to leaves to cue systemic defenses aboveground at later time points. Current evidence in maize (Zea mays) and tobacco (Nicotiana tabacum), as well as studies using Arabidopsis, suggest that roots are capable of synthesizing many secondary metabolites, serve as dynamic storage organs, and may also relay information regarding changes to their abiotic and biotic environment in a shoot-root-shoot loop in plant defense systems (Erb et al, 2009). Thus, future studies using short-lived isotopes with Arabidopsis may elucidate shoot-root and root-shoot signals that underlie carbon resource allocation and metabolic partitioning to plant defense chemistry to provide a better understanding of source-sink interactions in relation to plant defenses and their importance for pest resistance in other plant species.…”

Section: Resolving the Bunkering Conundrummentioning

confidence: 99%

Temporal Changes in Allocation and Partitioning of New Carbon as 11C Elicited by Simulated Herbivory Suggest that Roots Shape Aboveground Responses in Arabidopsis

et al. 2012

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Using the short-lived isotope 11C (t1/2 = 20.4 min) as 11CO2, we captured temporal changes in whole-plant carbon movement and partitioning of recently fixed carbon into primary and secondary metabolites in a time course (2, 6, and 24 h) following simulated herbivory with the well-known defense elicitor methyl jasmonate (MeJA) to young leaves of Arabidopsis (Arabidopsis thaliana). Both 11CO2 fixation and 11C-photosynthate export from the labeled source leaf increased rapidly (2 h) following MeJA treatment relative to controls, with preferential allocation of radiolabeled resources belowground. At the same time, 11C-photosynthate remaining in the aboveground sink tissues showed preferential allocation to MeJA-treated, young leaves, where it was incorporated into 11C-cinnamic acid. By 24 h, resource allocation toward roots returned to control levels, while allocation to the young leaves increased. This corresponded to an increase in invertase activity and the accumulation of phenolic compounds, particularly anthocyanins, in young leaves. Induction of phenolics was suppressed in sucrose transporter mutant plants (suc2-1), indicating that this phenomenon may be controlled, in part, by phloem loading at source leaves. However, when plant roots were chilled to 5°C to disrupt carbon flow between above- and belowground tissues, source leaves failed to allocate resources belowground or toward damaged leaves following wounding and MeJA treatment to young leaves, suggesting that roots may play an integral role in controlling how plants respond defensively aboveground.

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“…Under herbivory, wounding of plant tissues by insect feeding triggers the release of volatile signals that attract natural enemies of insects (Kessler and Baldwin, 2001). Upon insect infestation, plants release compounds such as hormones, exogenous volatile organic compounds, and secondary metabolites as long-distance root-to-shoot signals (for review, see Erb et al, 2009). Whitefly infestation of pepper (Capsicum annuum) plants elicits SAdependent signaling in leaves whereas roots showed increased colonization of Gram-positive bacterial populations (Yang et al, 2011), suggesting a signaling event between aboveground and belowground plant parts.…”

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confidence: 99%

Microbe-Associated Molecular Patterns-Triggered Root Responses Mediate Beneficial Rhizobacterial Recruitment in Arabidopsis

et al. 2012

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This study demonstrated that foliar infection by Pseudomonas syringae pv tomato DC3000 induced malic acid (MA) transporter (ALUMINUM-ACTIVATED MALATE TRANSPORTER1 [ALMT1]) expression leading to increased MA titers in the rhizosphere of Arabidopsis (Arabidopsis thaliana). MA secretion in the rhizosphere increased beneficial rhizobacteria Bacillus subtilis FB17 (hereafter FB17) titers causing an induced systemic resistance response in plants against P. syringae pv tomato DC3000. Having shown that a live pathogen could induce an intraplant signal from shoot-to-root to recruit FB17 belowground, we hypothesized that pathogen-derived microbe-associated molecular patterns (MAMPs) may relay a similar response specific to FB17 recruitment. The involvement of MAMPs in triggering plant innate immune response is well studied in the plant's response against foliar pathogens. In contrast, MAMPs-elicited plant responses on the roots and the belowground microbial community are not well understood. It is known that pathogen-derived MAMPs suppress the root immune responses, which may facilitate pathogenicity. Plants subjected to known MAMPs such as a flagellar peptide, flagellin22 (flg22), and a pathogen-derived phytotoxin, coronatine (COR), induced a shoot-to-root signal regulating ALMT1 for recruitment of FB17. Micrografts using either a COR-insensitive mutant (coi1) or a flagellin-insensitive mutant (fls2) as the scion and ALMT1 pro :b-glucuronidase as the rootstock revealed that both COR and flg22 are required for a graft transmissible signal to recruit FB17 belowground. The data suggest that MAMPs-induced signaling to regulate ALMT1 is salicylic acid and JASMONIC ACID RESISTANT1 (JAR1)/JASMONATE INSENSITIVE1 (JIN1)/MYC2 independent. Interestingly, a cell culture filtrate of FB17 suppressed flg22-induced MAMPsactivated root defense responses, which are similar to suppression of COR-mediated MAMPs-activated root defense, revealing a diffusible bacterial component that may regulate plant immune responses. Further analysis showed that the biofilm formation in B. subtilis negates suppression of MAMPs-activated defense responses in roots. Moreover, B. subtilis suppression of MAMPs-activated root defense does require JAR1/JIN1/MYC2. The ability of FB17 to block the MAMPselicited signaling pathways related to antibiosis reflects a strategy adapted by FB17 for efficient root colonization. These experiments demonstrate a remarkable strategy adapted by beneficial rhizobacteria to suppress a host defense response, which may facilitate rhizobacterial colonization and host-mutualistic association.

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The underestimated role of roots in defense against leaf attackers

Cited by 167 publications

References 93 publications

Integration of Biosynthesis and Long-Distance Transport Establish Organ-Specific Glucosinolate Profiles in VegetativeArabidopsis

Integration of Biosynthesis and Long-Distance Transport Establish Organ-Specific Glucosinolate Profiles in VegetativeArabidopsis

Temporal Changes in Allocation and Partitioning of New Carbon as 11C Elicited by Simulated Herbivory Suggest that Roots Shape Aboveground Responses in Arabidopsis

Microbe-Associated Molecular Patterns-Triggered Root Responses Mediate Beneficial Rhizobacterial Recruitment in Arabidopsis

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